Concerted evolution of body mass and cell size: similar patterns among species of birds (Galliformes) and mammals (Rodentia)

Abstract

Cell size plays a role in body size evolution and environmental adaptations. Addressing these roles, we studied body mass and cell size in Galliformes birds and Rodentia mammals, and collected published data on their genome sizes. In birds, we measured erythrocyte nuclei and basal metabolic rates (BMRs). In birds and mammals, larger species consistently evolved larger cells for five cell types (erythrocytes, enterocytes, chondrocytes, skin epithelial cells, and kidney proximal tubule cells) and evolved smaller hepatocytes. We found no evidence that cell size differences originated through genome size changes. We conclude that the organism-wide coordination of cell size changes might be an evolutionarily conservative characteristic, and the convergent evolutionary body size and cell size changes in Galliformes and Rodentia suggest the adaptive significance of cell size. Recent theory predicts that species evolving larger cells waste less energy on tissue maintenance but have reduced capacities to deliver oxygen to mitochondria and metabolize resources. Indeed, birds with larger size of the abovementioned cell types and smaller hepatocytes have evolved lower mass-specific BMRs. We propose that the inconsistent pattern in hepatocytes derives from the efficient delivery system to hepatocytes, combined with their intense involvement in supracellular function and anabolic activity.

Keywords: Allometry; BMR; Body size; Concerted evolution; Interspecific scaling; Karyoplasmic ratio; Metabolic rate; Optimal cell size; Species diversity.

Fig. 1.

In birds and mammals, larger species have evolved smaller hepatocytes but larger erythrocytes, chondrocytes, enterocytes, kidney cells and skin cells. Lines represent the standardized major axis (mammals: y=−2.36+1.159x; birds: y=−4.72+1.940x). Symbols represent the species means calculated from the data for five individuals and are marked with initials for each species name. Mammals: Ma, Microtus arvalis; Mc, Myocastor coypus; Mg, Myodes glareolus; Mm, Mus musculus; Ps, Phodopus sungorus; Rn, Rattus norvegicus. Birds: Ac, Alectoris chukar; Cc, Coturnix chinensis; Cj, Coturnix japonica; Pc, Phasianus colchicus; Pp, Perdix perdix. PC1 is the first principal component in the principal component analysis of cell size. Scores for PC1 were used to integrate information on the coordinated changes in cell size. Arrows indicate the loading values for cell size in different organs/tissues from PC1 (see Table 1), demonstrating the nature of cell size relationships.

Fig. 2.

In birds (A), the size of erythrocytes did not correlate with the size of erythrocyte nuclei, and in mammals (B), cell size did not correlate with genome size (C-value). Data about genome size (C-value; pg) were available for only two bird species, and they are shown in A near the initials of the species. C-values were not available for two species of mammals. Symbols are species means, marked with the initials for each species name. Panel A: Ac, Alectoris chukar; Cc, Coturnix chinensis; Cj, Coturnix japonica; Pc, Phasianus colchicus; Pp, Perdix perdix. Panel B: Mm, Mus musculus; Mc, Myocastor coypus; Ma, Microtus arvalis; Rn, Rattus norvegicus. PC1 is the first principal component in the principal component analysis of cell size. Scores for PC1 were used to integrate information on the coordinated changes in cell size. Arrows indicate loading values for cell size in different organs/tissues from PC1 (see Table 1), demonstrating the nature of cell size relationships.

Fig. 3.

In birds, metabolic rate increased allometrically with body mass (A) and birds with smaller hepatocytes and larger cells in the other five tissues sampled had lower mass-specific metabolic rates (B). Lines represent the standardized major axis (A: y=1.32+0.827x; B: y=7.11 −1.018x). Symbols are species means calculated from data for five individuals and are marked with the initials for each species name: Ac, Alectoris chukar; Cc, Coturnix chinensis; Cj, Coturnix japonica; Pc, Phasianus colchicus; Pp, Perdix perdix. PC1 is the first principal component in the principal component analysis of cell size. Scores for PC1 were used to integrate information on the coordinated changes in cell size. Arrows indicate loading values for cell size in different organs/tissues from PC1 (see Table 1), demonstrating the nature of cell size relationships.